• Non ci sono risultati.

Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles

N/A
N/A
Protected

Academic year: 2021

Condividi "Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles"

Copied!
32
0
0

Testo completo

(1)

24 July 2021

AperTO - Archivio Istituzionale Open Access dell'Università di Torino

Original Citation:

Acoustic communication within ant societies and its mimicry by mutualistic and socially parasitic myrmecophiles

Published version:

DOI:10.1016/j.anbehav.2016.10.031 Terms of use:

Open Access

(Article begins on next page)

Anyone can freely access the full text of works made available as "Open Access". Works made available under a Creative Commons license can be used according to the terms and conditions of said license. Use of all other works requires consent of the right holder (author or publisher) if not exempted from copyright protection by the applicable law. Availability:

This is the author's manuscript

(2)

Page 1 of 31 1

2 3 4

This is an author version of the contribution published on:

5

Questa è la versione dell’autore dell’opera:

6

[Animal Behaviour,

online first

, 10.1016/j.anbehav.2016.10.031]

7

8

The definitive version is available at:

9

La versione definitiva è disponibile alla URL:

10

[http://www.sciencedirect.com/science/article/pii/S0003347216302822]

11

12 13

(3)

Page 2 of 31

Acoustic communication within ant societies and its mimicry by

14

mutualistic and socially parasitic myrmecophiles

15

16

K Schönrogge1*, F. Barbero2, L.P. Casacci2, J Settele3, JA Thomas4

17 18 19 20 21

1. Centre for Ecology & Hydrology, MacLean Building, Benson Lane, Wallingford, OX10 22

8BB, UK 23

24

2. Department of Life Sciences and Systems Biology, University of Turin, Via Academia 25

Albertina, 10123, Turin, Italy 26

27

3. UFZ, Helmholtz Centre for Environmental Research, Department of Community Ecology, 28

Theodor-Lieser-Str. 4, 06120 Halle, Germany 29

30

4. Department of Zoology, University of Oxford, Oxford, South Parks Rd, OX1 3PS, United 31 Kingdom 32 33 34 35 36 37 38 39 40 41 * Corresponding author: 42

K. Schönrogge (ksc@ceh.ac.uk), Tel: +44 (0)1491 838800, Fax: +44 (0)1491 692424 43

44

Running title: Acoustic communication in ant – non-ant interactions 45

46

Word Count: 5390 (excl. references) 47

(4)

Page 3 of 31 Abstract:

49

This review focusses on the main acoustic adaptations that have evolved to enhance social 50

communication in ants. We also describe how other invertebrates mimic these acoustic 51

signals in order to coexist with ants in the case of mutualistic myrmecophiles, or, in the case 52

of social parasites, corrupt them in order to infiltrate ant societies and exploit their resources. 53

New data suggest that the strength of each ant-myrmecophile interaction leads to distinctive 54

sound profiles and may be a better predictor of the similarity of sound between different 55

myrmecophilous species than their phylogenetic distance. Finally, we discuss the 56

evolutionary significance of vibrations emitted by specialised myrmecophiles in the context of 57

ant multimodal communication involving the use of chemical and acoustic signals in 58

combination and identify future challenges for research including how new technology might 59

allow a yet better understanding of the study systems. 60

61 62

Keywords: Acoustic communication, ants, mutualists, social parasites, social structure 63

(5)

Page 4 of 31 Introduction

65

Efficient communication to coordinate the actions of up to a million specialised nestmates is 66

fundamental to the success of social insects, especially ants. Various modes of signalling 67

have been identified, including the release of semio-chemicals, visual behavioural displays 68

involving movement or posture, tactile interactions, and the comparatively poorly studied use 69

of acoustic signals (Hölldobler & Wilson, 1990, 2009). As hotspots of resources in their 70

environment, ants fiercely defend their colonies using a wide range of weapons (e.g. gland 71

secretions, mandibles, sting), which are deployed in the manner of co-ordinated attacks by 72

legions of intercommunicating workers. Nevertheless, ant nests are also magnets for other 73

organisms that have evolved means to overcome the hostility of the host ants. Thus, an 74

estimated ~10,000 invertebrate species live as obligate social parasites of ants, able to 75

penetrate and exploit the resources within host colonies in order to complete their life-cycle 76

(Thomas, Schönrogge, Elmes, 2005). The large majority of these adaptations evolved in 77

many separate lines, especially among Coleoptera, Diptera, Lepidoptera and other 78

Hymenoptera, from a ten-times greater number of commensals or mutualists (Fiedler, 1998; 79

Hölldobler & Wilson, 1990; Nash & Boomsma, 2008; Pierce et al., 2002; Thomas, 80

Schönrogge et al., 2005). All these myrmecophiles show morphological, behavioural, 81

chemical or acoustic adaptations to interact with ants (Cottrell, 1984; Donisthorpe, 1927; 82

Hinton, 1951; Lenoir, D'Ettorre, Errard, & Hefetz, 2001; Malicky, 1969; Wasmann, 1913; 83

Wheeler, 1910; Witek, Barbero, & Marko, 2014). Armour, stealth and the secretion of 84

attractive food rewards are frequently sufficient for unspecific or facultative myrmecophiles to 85

access the enemy-free spaces of ants. However, the subversion of the ants’ chemical and/or 86

acoustic signalling is generally required to enable true social parasites (sensu Nash & 87

Boomsma, 2008) to live for long periods as undetected intruders in close contact with their 88

hosts. 89

(6)

Page 5 of 31 A key element of successful co-habitation in ant nests is to circumvent the host’s ability to 90

differentiate between nestmates and intruders. Nestmate recognition is a dynamic process, 91

primarily based on the detection of distinctive species- or colony-specific cocktails of 92

cuticular hydrocarbons (CHC) covering the surface of all individuals (Hölldobler & Wilson, 93

1990; Howard, 1993; vander Meer & Morel, 1998; Winston, 1992). Social interactions such 94

as allogrooming ensure an exchange between the CHC mixtures among nestmates and give 95

rise to a shared CHC gestalt odour (vander Meer & Morel, 1998). The role that chemical 96

communication and nestmate recognition have in maintaining the cohesion of ant societies 97

and those of other social insects has been subject to extensive study, with excellent recent 98

reviews, for example by Martin & Drijfhout (2009) and van Wilgenburg, Symonds, & Elgar 99

(2011): The deployment of chemical communication by obligate social parasites to subvert 100

host recognition systems is equally well reviewed (e.g. Lenoir et al., 2001; von Thienen, 101

Metzler, Choe, & Witte, 2014). 102

In contrast, the function, the origin and role of acoustic signals in ants and their corruption by 103

social parasites are much less well studied. In this review, we therefore focus on the state of 104

the art concerning acoustic signaling in ants, and then consider the acoustic signaling of 105

obligate and facultative myrmecophiles. In both cases we emphasize the insights that have 106

resulted from recent technological advances that allow unalarmed ants and their guests to 107

be recorded and to receive broadcasts of their acoustic signals under semi-natural 108

conditions (Barbero, Thomas, et al., 2009; Riva, Barbero, Bonelli, Balletto, Casacci, in 109

press). 110

We first examine ant sound producing organs and convergent adaptations that allow non-ant 111

organisms to mimic and subvert ant–ant communications, focussing on advances in 112

knowledge since the reviews by Hölldobler & Wilson (1990), Fiedler (1998), Pierce and 113

colleagues (2002), Thomas and colleagues (2005) and Nash & Boomsma (2008), or covered 114

cursorily by Witek and colleagues (2014). We then review recent insights concerning the ant 115

acoustic signals themselves and their corruption by social parasites. This includes both the 116

(7)

Page 6 of 31 morphological adaptations to produce acoustic signals, the behavioural responses to them, 117

and thus the impact on ant – social parasite/guest interactions. Much of this builds on the 118

pioneering work of Markl (1965, 1967), DeVries (1991a, 1991b), Hölldobler, Braun, 119

Gronenberg, Kirchner, & Peeters (1994) and Kirchner (1997). Finally we present new data 120

relating the intimacy of interactions of lycaenid butterfly larvae to phylogeny and the similarity 121

of acoustic signalling. 122

Acoustic signalling in ants

123

The use of acoustics, whether through receiving pressure waves through the air (i.e. sounds 124

stricto sensu) or substrate vibrations, is a common means of communication in insects, 125

whose functions include defence, displays of aggression, territorial signalling and mate 126

attraction (Bennet-Clark, 1998; Gerhardt & Huber, 2002). Its advantage as a signal over 127

chemical volatiles lies in instantaneous reception that pinpoints a distant, but exact, location 128

to the receiver, for example in social insects to attract help (Markl, 1965, 1967; Roces, 129

Tautz, & Hölldobler, 1993). The physics, use and effects of substrate-borne vibrations of 130

ants and other insects are comprehensively reviewed by P.S. Hill (2009). A simple form 131

involves “drumming”, where the substrate is tapped by part of the exoskeleton to produce 132

vibrations. Drumming is employed by many ant taxa, but at least four of the eleven 133

subfamilies also stridulate by rasping a ‘plectrum’ across a ‘file’ (pars stridens), both 134

chitinous organs being located on opposite segments of the anterior abdomen (see Fig. 1 k-135

o, u-y) (Barbero, Thomas, Bonelli, Balletto, & Schönrogge, 2009b; Golden & P.S. Hill, 2016; 136

Ruiz, Martinez, Martinez, & Hernandez, 2006). Although these stridulations produce air-137

borne (as well as substrate-borne) pressure waves that are audible to the human ear, it 138

remains uncertain whether ants can perceive sound as pressure waves through the air 139

(Hickling & Brown, 2000, 2001; Roces & Tautz, 2001). In contrast, there is no controversy 140

about the ants’ ability to perceive substrate vibrations and two types of sensor have been 141

proposed to receive substrate vibrations: campaniform sensilla measuring the tension in the 142

(8)

Page 7 of 31 exoskeleton; and the subgenual organ, a spherical arrangement of sensory cells in the tibia, 143

as described from Camponotus ligniperda (Gronenberg, 1996; Menzel & Tautz, 1994). 144

Most studies that measure insect acoustics have used accelerometers, moving coil- or 145

particle velocity microphones, often with phase inversion focussing on the vibrational part of 146

the signal rather than pressure waves through the air. Hereafter in this review we use the 147

term “sound” sensu latu in its broadest sense, as we do the terms: calls, vibrations, vibro-148

acoustics and stridulations. 149

Early studies suggested that acoustic signals were a minor means of communication among 150

ants, largely confined to activities outside the nest and mainly signalling alarm or calls for 151

rescue, for instance when parts of nests collapse (Markl 1965, 1967). Due to a perceived 152

preponderance of stridulatory organs among soil nesting ant species, Markl (1973) 153

hypothesised that stridulation evolved initially as a burial/rescue signal when volatile 154

chemicals would be ineffective, whereas substrate borne vibrations would at least travel 155

short distances. However, this is not supported by Golden and P.S. Hill (2016), who showed 156

that stridulation organs have evolved independently multiple times in ants. In addition, 157

whereas Markl (1973) suggested that they would probably become vestigial over time in 158

arboreal ant species, due to the rarity of burial by soil, there was instead a strong positive 159

association between the presence of functional stridulation organs and the possession of an 160

arboreal life–style (Golden & P.S. Hill, 2016). 161

Nestmate recruitment is the most frequently reported function for ant–ant acoustic signalling. 162

For example, outside the nest, Atta cephalotes uses vibratory signals to attract foraging 163

workers towards newly found food sources (Roces & Hölldobler 1995). The same authors 164

also observed that in the presence of parasitic phorid flies, foragers used acoustics to recruit 165

minor workers for defence, thus also employing vibrations as alarm signals (Roces & 166

Hölldobler, 1995, 1996). Finally, although created by a scraper and file organ located on the 167

first gastric tergite and the post-petiole, Tautz and colleagues (1995) observed that 168

(9)

Page 8 of 31 vibrations travelled the length of the body to the mandibles, aiding the cutting of soft young 169

leaf tissue by stiffening it. Behavioural experiments, however, suggest that this is a 170

secondary effect and that communication is the main function for these vibrations (Roces & 171

Hölldobler, 1996). 172

It has recently become clear that acoustic signals are also used to transmit more abstract 173

information, including a species’ identity or an individual’s caste and status (Barbero, 174

Thomas et al., 2009; Casacci et al., 2013; Ferreira, Cros, Fresneau, & Rybak, 2014). For 175

example, modern molecular analyses revealed the neotropical ponerine ant species, 176

Pachycondyla apicalis, to be a species complex of five cryptic lineages. The stridulations of 177

three largely sympatric lineages are also distinctive, suggesting that morphological 178

characters on the pars stridens differ in length, width and ridge gap in each lineage (Ferreira, 179

Cros, Fresneau, & Rybak, 2014; Wild, 2005). By contrast, two allopatric lineages had very 180

similar acoustics, suggesting disruptive selection on this trait where sympatric overlap is 181

high. 182

Acoustic patterns also signal caste and hierarchical status in at least two genera of 183

Myrmicinae ants: Myrmica (Barbero, Thomas et al., 2009) and Pheidole (Di Giulio et al., 184

2015). In both taxa, the queens produce distinctive stridulations which, when played back to 185

kin workers, elicit additional ‘royal’ protective behaviours compared with responses to worker 186

signals (Barbero, Bonelli, Thomas, Balletto, & Schönrogge, 2009; Barbero & Casacci, 2015; 187

Barbero, Thomas et al., 2009; Casacci et al., 2013; Ferreira, Poteaux, Delabie, Fresneau, & 188

Rybak, 2010). In addition, in Pheidole pallidula the soldier and minor worker castes also 189

make distinctive vibroacoustic signals (Di Giulio et al., 2015). Unlike Pachycondyla species, 190

little inter-specific variation was detected in either the queen- or worker-sounds made by 191

closely-related sympatric species of Myrmica (Barbero et al., 2012; Barbero, Thomas et al., 192

2009; Thomas, Schönrogge, Bonelli, Barbero, & Balletto, 2010), which are instead clearly 193

demarcated by unique hydrocarbon profiles (Elmes, Akino, Thomas, Clarke, & Knapp, 194

(10)

Page 9 of 31 2002). Although the young stages of tested ants are mute (e.g. DeVries, Cocroft, & Thomas, 195

1993), Casacci and colleagues (2013) found that acoustic signalling appears to act as a 196

substitute for other forms of communication in developing Myrmica pupae. The various 197

stages of ant brood, from egg to pupa, are afforded ascending levels of priority based on 198

tactile and chemical cues (Brian, 1975). Most are mute, but the older “brown”, sclerotised 199

pupae of Myrmica species produce calls, emitted as single pulses, similar to those of 200

workers (Casacci et al. 2013). This coincides with a presumed reduced ability to secrete 201

brood recognition pheromones during this period, and brown pupae that were experimentally 202

silenced fell significantly behind their mute white siblings in social standing. 203

Acoustic signals of myrmecophiles

204

Derived acoustic signals that enhance interactions with ants are increasingly being 205

confirmed in both juvenile and adult stages of myrmecophiles. To date, most studies involve 206

riodinid and, especially, lycaenid butterfly larvae and pupae (e.g. Barbero, Thomas et al., 207

2009; DeVries, 1990, 1991a; Pierce et al., 2002). However, similar phenomena were 208

recently described from adults of a socially parasitic beetle, Paussus favieri (Di Giulio et al., 209

2015), where males and females emit mimetic stridulations using a row of scrapers on the 210

proximal abdominal segment rasping across a file located on the hind femora (see Fig. 1p-t). 211

Stridulation organs 212

With a few exceptions, an ability to produce calls occurs after the third larval moult in riodinid 213

and lycaenid larvae, coinciding with the development of chemical ‘ant organs’, which 214

perhaps suggests they act synergistically (DeVries, 1991a). In most riodinids, acoustic 215

signals are generated by grooved vibratory papillae. These are typically found in pairs on the 216

prothorax, and grate against specialised epicranial granulations when the larva rotates its 217

head (see Fig 1a-e), especially when walking or under attack, generating low amplitude 218

substrate-borne calls (DeVries, 1991a). The tribe Eurybiini lacks vibratory papillae; instead, 219

(11)

Page 10 of 31 caterpillars generate calls by scraping teeth on a prothoracic cervical membrane against the 220

epicranial granulations in at least some mutualists or entomophagous predators of ant-221

tended Homoptera (DeVries & Penz, 2002; Travassos, DeVries, & Pierce, 2008). The 222

detection of dedicated organs in lycaenid larvae that produce calls has been elusive, apart 223

from a file-and-scraper described between the 5th and 6th abdominal segments of Arhopala

224

madytus (C. J. Hill, 1993) and a putative organ in Maculinea rebeli larvae (see Fig.1fg). In 225

other species strong substrate-borne vibrations (and apparently weak air-borne sounds) may 226

be generated by muscular contractions of the abdomen, which compress air through the 227

tracheae to produce distinctive rhythms and intensities in the manner of a wind instrument, 228

as described by Schurian and Fiedler (1991) for Polyommatus dezinus. These vibroacoustic 229

signals range from low background calls punctuated by pulses in mutualists (DeVries, 230

1991a) to the grunts, drumming and hisses of the host-specific Jalmenus evagoras 231

(Travassos & Pierce, 2000), to the mimetic calls of Maculinea larvae (Barbero, Bonelli et al., 232

2009; DeVries et al., 1993; Sala, Casacci, Balletto, Bonelli, & Barbero, 2014). 233

In contrast, the pupae of all lycaenids studied (Pierce et al., 2002) and a minority of riodinids 234

(DeVries, 1991a; Downey & Allyn, 1973; 1978; Ross, 1966) have a well-developed file-and-235

scraper organ (two pairs in the case of riodinids) situated between opposite segments of the 236

abdomen, that emit substrate- and air-borne calls often audible to humans (see Fig 1h-j). In 237

lycaenids, the plate against which teeth are rubbed may be complex, consisting of tubercles, 238

reticulations or ridges (Alvarez, Munguira, & Martinez-Ibanez, 2014). 239

Acoustic signalling in ant–myrmecophile interactions 240

Evidence that the acoustics of myrmecophiles are adaptive to their interactions with ants has 241

progressed from correlative studies to two experimental approaches: muting the 242

myrmecophile or recording and playing back their calls to undisturbed ant colonies. 243

First, DeVries (1991c) showed that fewer ants attended larvae of the mutualistic riodinid 244

Thisbe irenea that had been artificially silenced compared with controls that were able to 245

(12)

Page 11 of 31 call, establishing that at least one function of riodinid calls is to attract ants. Similarly, 246

Travassos and Pierce (2000) demonstrated that pupae of the lycaenid Jalmenus evagoras 247

stridulated more frequently in the presence of Iridomyrmex anceps ants, and attracted and 248

maintained a larger number of guards than muted ones. The calls convey the pupa’s value 249

as a provider of nutritious secretions to the ants, which does however, represent a significant 250

cost to the pupae. Tended pupae have been shown to lose 25% of weight and take longer to 251

eclose than untended ones (Pierce, Kitching, Buckley, Taylor, & Benbow, 1987). In further 252

behavioural experiments Travassos and Pierce (2000) showed that pupae used acoustic 253

signalling to adjust the number of attendant ants. They provided a path from an I. anceps 254

nest to signalling pupae and scored the rate of worker movement in relation to signal 255

strength once the pupa was discovered. This appears to be an important fitness component 256

evolved to attract no more than an adequate number of ant guards against enemy attacks. 257

The larvae of J. evagoras produce more varied acoustic signals than pupae - grunts, hisses 258

and drumming – and are also heavily attended and guarded by their mutualist ant (Pierce et 259

al., 2002). Hisses are emitted briefly after encountering a worker, whereas grunts are 260

produced throughout ant attendance. The ability of J. evagoras juveniles to produce distinct 261

vibrations, some probably with different functions, suggests the evolution of a finely-tuned 262

acoustic system of communication with their hosts, which might be elucidated using play-263

back experiments. 264

In parasitic interactions with ant colonies, the clearest evidence to date that some acoustic 265

signals are mimetic involves the highly specialized species of the Myrmica ant - Maculinea 266

butterfly and Pheidole ant - Paussus beetle systems. Initially, DeVries and colleagues (1993) 267

showed that the calls made by larvae of four Maculinea species differed from those of 268

phytophagous lycaenids in showing distinctive pulses that resembled the stridulations of 269

Myrmica worker ants. This was the first suggestion of mimicry of an adult host attribute by 270

the caterpillars, which appeared to be genus- rather than species-specific. The insects in 271

early experiments were unavoidably alarmed, being held with forceps during the recording, 272

(13)

Page 12 of 31 but a similar genus-specific result was later obtained using modern equipment and 273

unstressed ants and butterflies. Both the pupae and larvae of Maculinea species closely 274

mimicked three attributes of their hosts’ acoustic signals: dominant frequency, pulse length, 275

pulse repetition frequency (Barbero, Bonelli et al., 2009, Barbero, Thomas et al., 2009). 276

However, the calls of both stages were significantly more similar to queen ant calls than they 277

were to worker calls, despite each being generated in a different way (see Fig.1f-j). 278

Behavioural bioassays, where the calls of butterflies and ants were played back to 279

unstressed Myrmica workers, revealed that the calls of juvenile Maculinea, especially those 280

of pupae, caused workers to respond as they do to queen ant calls. Both types of acoustic 281

stimuli caused worker ants to aggregate, antennate the source of sound, and show 282

significantly higher levels of guarding behaviour than was elicited in response to worker ant 283

calls (Barbero, Thomas et al., 2009). 284

Similar, but more sophisticated communication, was recently described between the carabid 285

beetle Paussus favieri, an obligate social parasite in all stages of its life-cycle, and their host 286

ant Pheidole pallidula (Di Giulio et al., 2015). Here the adult beetle can generate three types 287

of call when it stridulates, which respectively mimic the calls made by the queens, the 288

soldiers and the minor worker caste of its host. These calls elicit a range of responses when 289

played back to worker ants, consistent with the intruder’s more diverse activities (compared 290

to juvenile Maculinea) in different parts of the host’s society and nest. Thus P. favieri’s 291

various stridulations can elicit recruitment, including digging (rescue) behaviour, as well as 292

the enhanced level of ‘royal’ (queen ant) protection observed towards Maculinea pupae and 293

larvae. 294

[insert Figure 1] 295

Larval acoustic signals and phylogeny in the Lycaenidae 296

Various authors (e.g. DeVries, 1991a, 1991b; Fiedler, 1998; Pech, Fric, Konvicka, & Zrzavy, 297

2004; Pellissier, Litsios, Guisan, & Alvarez, 2012; Pierce et al., 2002) have analysed the 298

(14)

Page 13 of 31 evolution of myrmecophily in lycaenids and riodinids, including social parasitism in the 299

Lycaenidae, and most concluded that it also provided a template for diversification and 300

radiation in these species-rich families. Pierce and colleagues (2002) argued convincingly 301

that social parasitism (including entomophagy of the domestic Hemiptera of ants) has 302

evolved independently in at least 20 lineages. 303

The analysis of acoustics as a parameter in evolutionary studies of these taxa was 304

pioneered by DeVries (1991a, 1991b). In seminal early papers, DeVries (1991a, 1991b) 305

found that only lycaenids and riodinids that interacted with ants produced calls, while several 306

non myrmecophilous members of the tribe Eumaeini were silent. Subsequent studies and 307

reviews confirmed this pattern (e.g. Fiedler, Seufert, Maschwitz, & Idris, 1995) and provided 308

evidence of the use of lycaenid calls in enhancing the interaction with ants (Pierce et al., 309

2002; Barbero, Thomas et al., 2009, Sala et al. 2014). However, some lycaenid and riodinid 310

larvae and pupae also emit sounds when disturbed by putative predators or parasitoids, 311

even if ants are absent. In addition, other species classed as having no interaction with ants 312

do emit sound (e.g. Alvarez et al., 2014; Downey & Allyn, 1973; 1978; Fiedler, 1992, 1994; 313

Schurian & Fiedler, 1991). The most recent study, by Riva and colleagues (in press), found 314

that lycaenid sounds are highly specific and are emitted by both non- and myrmecophilous 315

species. Calls by species that are least associated with ants consist of shorter and more 316

distant pulses relative to those of species that are highly dependent on them. 317

Here we further explore the hypothesis that the strength of ant-myrmecophile interactions 318

(using Fiedler’s 1991 definitions) leads to characteristic sound profiles that may be a better 319

predictor of the similarity of sound between species than their phylogenetic distance. We 320

present a new analysis of the acoustic profiles made by 13 species of European lycaenids, 321

ranging from highly integrated ‘cuckoo’ social parasites (Maculinea alcon, Ma. rebeli) via one 322

host-specific mutualist (Plebejus argus) and a spectrum of generalist myrmecophiles, to 323

species for which little or no interaction is known (Lycaena spp.). The 13 species (see Fig. 2) 324

are a subset of the commensal or mutualistic species used by Riva and colleagues (in 325

(15)

Page 14 of 31 press), with three species of Maculinea added to represent the two levels of intimate 326

integration found in this socially parasitic genus (Thomas, Schönrogge et al., 2005). 327

Fourth instar caterpillars were recorded using customized equipment, as described by Riva 328

and colleagues (in press). We analyzed recordings of three individuals per species, 329

randomly selecting two trains of five pulses in each trace. Fourteen sound parameters were 330

measured using Praat v. 5.3.53 (Boersma & Weenink, 2013). These included the lower and 331

higher quartiles of the energy spectrum (Hz), power (dB2), intensity (dB), the

root-mean-332

square intensity level (dB) and the relation of the frequency peak energy to the call total 333

energy (%). Two temporal variables were measured from the oscillogram: the duration of the 334

pulse (s) and the Pulse Rate (calculated as 1/tstart(x) - tstart(x+1); s-1). Six additional variables

335

were estimated on each pulse by inspection of power spectra: the frequency of the first, 336

second and third peak amplitudes (Hz), the intensity of the first two peaks (dB) and the 337

center of gravity (Hz). 338

Hierarchical Cluster analyses was performed on a matrix of normalized Euclidean distances 339

over sound parameters, averaged by individual using unweighted pair-group average 340

(UPGMA) in Primer v. 6.1.12 (Primer-E Ltd.). A two-sample t - test was used to compare 341

differences between group distances.To test whether species differences reflect degrees of 342

myrmecophily, we used Phylogenetic Regression as implemented in the library “phyreg” 343

(Grafen, 1989) using R (R Core Team, 2015). Principal components, derived by PCA on log-344

transformed sound parameters, were correlated with the degree of myrmecophily while 345

controlling for phylogenetic relatedness among species. To assemble a working phylogeny, 346

we used cytochrome oxidase subunit 1 (COI) sequences of the 13 lycaenid species from two 347

recent studies on the Romanian and Iberian butterflies (Dinca et al., 2015; Dinca, Zakharov, 348

Hebert, & Vila, 2011). Geneious Pro 4.7.5 (Biomatters, http://www.geneious.com/) was used 349

to align COI sequences and to produce a neighbor-joining (NJ) tree. We also included in the 350

phylogeny Hamearis lucina (Riodinidae) and Pieris rapae (Pieridae) as outgroups. 351

(16)

Page 15 of 31 Two trees for species’ phylogenetic distance and for the similarity of acoustic profiles are 352

presented in Figure 2, together with the score for myrmecophily of each species. Similarities 353

in sound profiles neatly match the spectrum of observed strengths and specificities in 354

myrmecophily across the study species, much more closely than does phylogeny. Overall, 355

PC1 of the acoustic parameters explained 56% and PC2 a further 27% of variation, and both 356

were significantly correlated with the differences in myrmecophilous relationships (PC1: F1,13

357

= 11.146, P = 0.005; PC2: F1,13 = 6.959, P = 0.020) after accounting for phylogeny using

358

phylogenetic regression. 359

It is apparent that the sound profiles of Ma. rebeli and Ma. alcon (average Euclidean 360

distance (± 1SD) between Ma. rebeli and Ma. alcon = 1.65 ± 0.14) are far removed from all 361

other species, including from their congeners Ma. arion and Ma. teleius (Barbero, Bonelli et 362

al., 2009; Sala et al., 2014). Indeed, the mean Euclidean distances in the acoustic signals of 363

Ma. alcon or Ma. rebeli from other lycaenid species are among the highest measured to date 364

(mean Euclidean acoustic distance of Ma. alcon vs. lycaenids other than M. rebeli: 7.41 ± 365

1.00; Ma. rebeli vs lycaenids other than Ma. alcon: 7.66 ± 1.01; see also Riva et al. in press). 366

This is consistent with the intimate level of social integration these species achieve within 367

host ant nests, an association that is so close that in times of shortage the ants kill their own 368

brood to feed to these ‘cuckoos’ in the nest (Thomas, Elmes, Schönrogge, Simcox, & 369

Settele, 2005). It is also notable that the acoustics of Plebejus argus, the only host-specific 370

myrmecophile among the mutualistic species, is less similar to its nearest relative Plebejus 371

argyrognomon, and appears to converge with the two ‘predatory’ Maculinea social parasites 372

even though its ‘host’ ant, Lasius niger, has no known stridulation organs and belongs to a 373

different subfamily to Myrmica (mean Euclidean acoustic distance of P. argus vs. P. 374

argyrognomon: 4.33 ± 0.30; P. argus vs M. arion: 2.51 ± 0.55; paired t test: t16 = -8.723, P <

375

0.001; distance of P. argus vs. Ma. teleius: 3.79 ± 0.28; paired t test: t16 = -3.963, P = 0.001).

376

Scolitantides orion perhaps represents selection in the opposite direction to P. argus, being 377

less host specific than its ancestry or relatives might suggest, as, less convincingly, may 378

(17)

Page 16 of 31 Polyommatus icarus. Yet despite L. coridon and L. bellargus being close congeners, sounds 379

emitted by L. bellargus are much more similar to those produced by P. argyrognomon 380

(belonging to the same myrmecophilous category - 3) rather than to L. coridon (mean 381

Euclidean acoustic distance of L. coridon vs L. bellargus: 3.87 ± 0.15; P. argyrognomon vs L. 382

bellargus: 1.54 ± 0.20; paired t test: t16 = 27.775, P < 0.001). A possible, but untested,

383

explanation is that this reflects a similar disruptive selection via acoustics to that described in 384

sympatric lineages of the ant Pachycondyla, since the juveniles of these congeneric 385

butterflies overlap largely in distribution, sharing the same single species of foodplant and 386

often the same individual plant. 387

However, given the small number of species studied, we caution against over-interpreting 388

the apparent patterns depicted in Figure 2, and suggest they be tested by comparative 389

behavioural experimentation. We also recognise that vibrations of less- or non-390

myrmecophilous lycaenids (and other taxa) may have very different functions, such as 391

repelling natural enemies (Bura, Fleming, & Yack, 2009; Bura, Rohwer, Martin, & Yack, 392

2011). We tentatively suggest that ancestral species in the Lycaenidae were preadapted to 393

myrmecophily through an ability to make sounds, and that once behavioural relationships 394

with ants evolved, the selection regime changed resulting in adaptive mimetic sound profiles, 395

at least among obligate myrmecophiles. 396

[insert Figure 2] 397

Conclusions & Future Research

398

Ants are known to sometimes use multiple cues to moderate kin behaviour, for example by 399

combining posturing, tactile and chemical interactions to convey complex or sequential 400

information and to elicit particular responses between members of their society (Hölldobler & 401

Wilson, 1990). To date little is known of how acoustic signalling might interact with other 402

(18)

Page 17 of 31 means of communication, and less still of whether myrmecophiles manipulate behaviour 403

using multiple cues. 404

Sound may be used synergistically with other modes of signalling. Hölldobler and colleagues 405

(1994) studied the role of audible vibrational signals made by the Ponerine ant Megaponera 406

foetens, a raider of termite colonies, in the context of trail following and column building.

407

They found that stridulations were emitted only during disturbances and for predator 408

avoidance. It is also known that M. foetens has a distinctive pheromone to signal alarm 409

(Janssen, Bestmann, Hölldobler, & Kern, 1995). These observations suggest that vibrations 410

may be used to qualify a general alarm signal that is chemical, but again this requires formal 411

testing. This is in contrast to the observations by Casacci and colleagues (2013) described 412

above where acoustic signalling appears to replace chemical and tactile signal apparently 413

with the same function of signalling rank, but this is not truly a case of multimodal 414

communication. 415

To date, no direct evidence exists for the behavioural consequences of full synergistic 416

multimodal communication involving acoustics. Yet the interactions of Maculinea butterfly 417

larvae and their Myrmica host ant societies illustrate the importance of both chemical and 418

acoustic mimicry. Here, the acceptance (or rejection) of larvae as members of their host 419

colony appears to be based entirely on a mimetic mixture of chemical secretions, but on this 420

cue alone intruders are treated simply like the low-ranking kin brood (Akino, Knapp, Thomas, 421

& Elmes, 1999; Thomas et al., 2013; Thomas, Schönrogge et al., 2005). It is the ability 422

simultaneously to emit acoustic calls that mimic adult hosts, and furthermore mimic queen 423

sounds, that is believed to explain the observed priority ‘royal’ behaviour that workers 424

regularly afford to social parasites, giving them a status that exceeds that of large ant larvae. 425

Not only do these brood parasites gain priority in the distribution of food by nursery workers 426

to the extent that workers feed younger kin ant brood to the Maculinea larvae when food is 427

short, but they are also carried ahead of kin ant brood when moving nest or during rescues 428

(19)

Page 18 of 31 (Elmes, 1989; Gerrish, 1994; Thomas, Schönrogge, et al., 2005). Anecdotal observations of 429

the manipulation of Paussus favieri by the beetle Pheidole pallidula suggests a similar 430

chemical-acoustic mechanism (Di Giulio et al., 2015), but as with ant-ant communication 431

itself, the putative use of acoustics in multimodal communication requires rigorous testing. 432

About 10,000 species of invertebrates from 11 orders are estimated have evolved 433

adaptations to infiltrate ant societies and live as parasites inside nests (Hölldobler & Wilson, 434

1990). Current studies have largely focussed on the family Lycaenidae among the 435

Lepidoptera and a few selected species of Coleoptera. While the study systems used today 436

provide some variety in the type of interactions with their host ants, there is clearly a vast 437

variety still to be discovered to understand respective roles of signalling modes and the 438

social interactions in ants and other social insects. 439

The important role that acoustic signalling has in ant- and other social insect societies is well 440

established and it is perhaps unsurprising that other, interacting species show adaptations 441

that relate to the hosts acoustic traits. In only a few cases, however, has the role of vibro-442

acoustics in mediating myrmecophile - host interactions been investigated experimentally. 443

The modalities of signal production, transmission and reception remain largely unknown for 444

most species of myrmecophiles or indeed their hosts, but the greatest future challenge is to 445

understand how different modes of signalling interact. Social insects are well known to 446

interpret stimuli in a context-dependent manner, where the same stimulus can trigger a 447

different behaviour when encountered under different circumstances (Hölldobler & Wilson 448

1990). Other aspects of insect social behaviour have been subject to sophisticated and 449

successful experimentation, and it should be possible to unravel this essential aspect of 450

communication. Hunt and Richards (2013) suggested that understanding the suites of 451

modalities in signalling enables a clearer view of the adaptive role of multimodal 452

communication, and while that has been true for rare examples such as the honey bee 453

waggle dance, research into understanding the role of ant acoustics is in its infancy. With the 454

development of recording equipment that is portable, affordable, which can focus on 455

(20)

Page 19 of 31 individuals and record sound and behaviour at the same time, our understanding of social 456

interactions should become more specific. Such instruments, laser-vibrometers and hand-457

held “noses” for acoustic and chemical analyses, are being developed for engineering 458

applications and could be deployed to record acoustic and chemical signals in behavioural 459

science in the near future. Technological developments in both recording equipment and 460

behavioural experimentation will allow designing studies following the same principles to 461

investigate synergistic effects of multiple chemical signals. 462

Acknowledgments 463

The authors collaborated within the project CLIMIT (Climate Change Impacts on Insects and 464

their Mitigation), funded by Deutsches Zentrum für Luft-und Raumfahrt-Bundesministerium 465

für Bildung und Forschung (Germany); Natural Environment Research Council (NERC) and 466

Department for Environment, Food, and Rural Affairs (UK); Agence nationale de la 467

recherche (France); Formas (Sweden); and Swedish Environmental Protection Agency 468

(Sweden) through the FP6 BiodivERsA Eranet. Part of the research was funded by the 469

Italian Ministry of Education, University, and Research (MIUR) within the project ‘‘A multitaxa 470

approach to study the impact of climate change on the biodiversity of Italian ecosystems.’ 471

Ethical Note 472

The authors confirm that their work adheres to the ASAB/ABS and ARRIVE Guidelines. The 473

guide to ethical information required for papers published in the journal has been consulted 474

as well. Maculinea caterpillars were collected under permit from The Italian Ministry for the 475

Environment (protocol numbers: 446/05. DPN/2D/2005/13993 & 0012494/PNM/2015). 476

The authors declare that there is no conflict of interest. 477

References

478

Akino, T., Knapp, J. J., Thomas, J. A., & Elmes, G. W. (1999). Chemical mimicry and host 479

specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. 480

(21)

Page 20 of 31 Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 481

1419-1426. 482

Alvarez, M., Munguira, M. L., & Martinez-Ibanez, M. D. (2014). Comparative study of the 483

morphology of stridulatory organs of the Iberian lycaenid butterfly pupae 484

(Lepidoptera). Journal of Morphology, 275, 414-430. 485

Barbero, F., Bonelli, S., Thomas, J. A., Balletto, E., & Schönrogge, K. (2009a). Acoustical 486

mimicry in a predatory social parasite of ants. Journal of Experimental Biology, 212, 487

4084-4090. 488

Barbero, F., & Casacci, L. P. (2015). Butterflies that trick ants with sound. Physics Today, 489

68, 64-65. 490

Barbero, F., Patricelli, D., Witek, M., Balletto, E., Casacci, L. P., Sala, M., & Bonelli, S. 491

(2012). Myrmica ants and their butterfly parasites with special focus on the acoustic 492

communication. Psyche: A Journal of Entomology, 2012, 1-11. 493

Barbero, F., Thomas, J. A., Bonelli, S., Balletto, E., & Schönrogge, K. (2009). Queen ants 494

make distinctive sounds that are mimicked by a butterfly social parasite. Science, 495

323, 782-785. 496

Bennet-Clark, H. C. (1998). Size and scale effects as constraints in insect sound 497

communication. Philosophical Transactions of the Royal Society B, 353, 407 - 419. 498

Boersma, P., & Weenink, D. (2013). Praat: Doing phonetics by computer [Computer 499

program]. Version 5.3.53. (2013) retrieved from http://www.praat.org. 500

Brian, M. V. (1975). Larval recognition by workers of the ant Myrmica. Animal Behaviour, 23, 501

745 - 756. 502

Bura, V. L., Fleming, A. J., & Yack, J. E. (2009). What's the buzz? Ultrasonic and sonic 503

warning signals in caterpillars of the great peacock moth (Saturnia pyri). 504

Naturwissenschaften, 96, 713-718. 505

Bura, V. L., Rohwer, V. G., Martin, P. R., & Yack, J. E. (2011). Whistling in caterpillars 506

(Amorpha juglandis, Bombycoidea): sound-producing mechanism and function. The 507

Journal of Experimental Biology, 214, 30-37. 508

(22)

Page 21 of 31 Casacci, L. P., Thomas, J. A., Sala, M., Treanor, D., Bonelli, S., Balletto, E., & Schönrogge, 509

K. (2013). Ant Pupae Employ Acoustics to Communicate Social Status in Their 510

Colony’s Hierarchy. Current Biology, 23, 323-327. 511

Cottrell, C. B. (1984). Aphytophagy in Butterflies - Its Relationship to Myrmecophily. 512

Zoological Journal of the Linnean Society, 80, 1-57. 513

DeVries, P. J. (1990). Enhancement of symbioses between butterfly caterpillars and ants by 514

vibrational communication. Science, 248, 1104-1106. 515

DeVries, P. J. (1991a). Call production by myrmecophilous riodinid and lycaenid butterfly 516

caterpillars (Lepidoptera): morphological, acoustical, functional, and evolutionary 517

patterns. American Museum Novitates, 3025, 1-23. 518

DeVries, P. J. (1991b). Evolutionary and Ecological Patterns in Myrmecophilous-Riodinid 519

Butterflies. In C. R. Huxley & D. F. Cutler (Eds.), Ant - Plant Interactions (pp. 143-520

156). Oxford: Oxford University Press. 521

DeVries, P. J. (1991c). Mutualism between Thisbe irenae butterflies and ants, and the role of 522

ant ecology in the evolution of larval - ant associations. Biological Journal of the 523

Linnean Society, 43, 179 - 195. 524

DeVries, P. J., Cocroft, R. B., & Thomas, J. A. (1993). Comparison of acoustical signals in 525

Maculinea butterfly caterpillars and their obligate host Myrmica ants. Biological 526

Journal of the Linnean Society, 49, 229-238. 527

DeVries, P. J., & Penz, C. M. (2002). Early stages of the entomophagous metelmark 528

butterfly Alesa amesis (Riodinidae: Eurybiini). Journal of the Lepidopterist's Society, 529

56, 265 - 271. 530

Di Giulio, A., Maurizi, E., Barbero, F., Sala, M., Fattorini, S., Balletto, E., & Bonelli, S. (2015). 531

The Pied Piper: A Parasitic Beetle's Melodies Modulate Ant Behaviours. PLoS One, 532

10, e0130541. doi: 10.1371/journal.pone.0130541 533

Dinca, V., Montagud, S., Talavera, G., Hernandez-Roldan, J., Munguira, M. L., Garcia-534

Barros, E., Hebert, P.D.N, & Vila, R. (2015). DNA barcode reference library for 535

(23)

Page 22 of 31 Iberian butterflies enables a continental-scale preview of potential cryptic diversity. 536

Scientific Reports, 5. 537

Dinca, V., Zakharov, E. V., Hebert, P. D. N., & Vila, R. (2011). Complete DNA barcode 538

reference library for a country's butterfly fauna reveals high performance for 539

temperate Europe. Proceedings of the Royal Society B-Biological Sciences, 278, 540

347-355. 541

Donisthorpe, H. S. J. K. (1927). The Guests of British Ants. London: Routledge. 542

Downey, J. C., & Allyn, A. C. (1973). Butterfly ultrastructure: 1. Sound production and 543

associated abdominal structures in pupae of Lycaenidae and Riodinidae. Bulletin of 544

the Allyn Museum, 14, 1-47. 545

Downey, J. C., & Allyn, A. C. (1978). Sounds produced in pupae of Lycaenidae. Bulletin of 546

the Allyn Museum, 48, 1-14. 547

Elmes, G. W. (1989). The effect of multiple queens in small groups of Myrmica rubra L. 548

Actes colloquia. Insectes Sociaux, 5, 137 - 144. 549

Elmes, G. W., Akino, T., Thomas, J. A., Clarke, R. T., & Knapp, J. J. (2002). Interspecific 550

differences in cuticular hydrocarbon profiles of Myrmica ants are sufficiently 551

consistent to explain host specificity by Maculinea (large blue) butterflies. Oecologia, 552

130, 525-535. 553

Ferreira, R. S., Cros, E., Fresneau, D., & Rybak, F. (2014). Behavioural Contexts of Sound 554

Production in Pachycondyla Ants (Formicidae: Ponerinae). Acta Acustica united with 555

Acustica, 100, 739-747. 556

Ferreira, R. S., Poteaux, C., Delabie, J. H., Fresneau, D., & Rybak, F. (2010). Stridulations 557

reveal cryptic speciation in neotropical sympatric ants. PLoS One, 5, e15363. 558

Fiedler, K. (1991). Systematic, evolutionary, and ecological implications of myrmecophily 559

within the Lycaenidae (Insecta: Lepidoptera: Papilionoidea). Bonner Zoologische

560

Monographien, 31, 1-210

(24)

Page 23 of 31 Fiedler, K. (1992). Notes on the biology of Hypo/yeaena otbona (Lepidoptera: Lycaenidae) In 562

West Malaysia. Nachrichten des entomologischen Vereins Apollo, Frankfurt. NF, 13, 563

65-92. 564

Fiedler, K. (1994). Lycaenid butterflies and plants: is myrmecophily associated with amplified 565

hostplant diversity? Ecological Entomology, 19, 79-82. 566

Fiedler, K. (1998). Geographical patterns in life-history traits of Lycaenidae butterflies - 567

ecological and evolutionary patterns. Zoology, 100, 336 - 347. 568

Fiedler, K., Seufert, P., Maschwitz, U., & Idris, A. H. J. (1995). Notes on larval biology and 569

pupal morphology of Malaysian Curetis butterflies(Lepidoptera: Lycaenidae). 570

Transactions of the Lepidopterological Society of Japan, 45, 287-299. 571

Gerhardt, H. C., & Huber, F. (2002). Acoustic communication in insects and anurans: 572

common problems and diverse solutions: University of Chicago Press. 573

Gerrish, A. R. (1994). The influence of relatedness and resource investment on the 574

behaviour of worker ants towards brood. PhD, University of Exeter, Exeter, UK. 575

Golden, T. M. J., & Hill, P. S. (2016). The evolution of stridulatory communication in ants, 576

revisited. Insectes Sociaux, 63, 309-319. 577

Grafen, A. (1989). The Phylogenetic Regression. Philosophical Transactions of the Royal 578

Society of London Series B-Biological Sciences, 326, 119-157. doi: 579

10.1098/rstb.1989.0106 580

Gronenberg, W. (1996). Neuroethology of ants. Naturwissenschaften, 83, 15-27. 581

Hickling, R., & Brown, R. L. (2000). Analysis of acoustic communication by ants. Journal of 582

the Acoustical Society of America, 108, 1920-1929. 583

Hickling, R., & Brown, R. L. (2001). Response to "Ants ar deaf". Journal of the Acoustical 584

Society of America, 109, 3083. 585

Hill, C. J. (1993). The myrmecophilous organs of Arhopala madytus Fruhstorfer 586

(Lepidoptera: Lycaenidae). Australian Journal of Entomology, 32, 283-288. 587

Hill, P. S. (2009). How do animals use substrate-borne vibrations as an information source? 588

Naturwissenschaften, 96, 1355-1371. 589

(25)

Page 24 of 31 Hinton, H. E. (1951). Myrmecophilous Lycaenidae and other Lepidoptera - a summary. 590

Proceedings & Transactions of the South London Entomological and Natural History 591

Society, 1949-50, 111 - 175. 592

Hölldobler, B., Braun, U., Gronenberg, W., Kirchner, W. H., & Peeters, C. (1994). Trail 593

Communication in the Ant Megaponera Foetens (Fabr) (Formicidae, Ponerinae). 594

Journal of Insect Physiology, 40, 585-593. 595

Hölldobler, B., & Wilson, E. O. (1990). The ants. Berlin Heidelberg: Springer Verlag. 596

Hölldobler, B., & Wilson, E. O. (2009). The superorganism: the beauty, elegance, and 597

strangeness of insect societies. London: WW Norton & Company. 598

Howard, R. W. (1993). Cuticular Hydrocarbons and Chemical Communication. In D. W. 599

Stanley-Samuelson & D. R. Nelson (Eds.), Insect Lipids: Chemistry, Biochemistry 600

and Biology (pp. 179 - 226). Lincoln: University of Nebraska Press. 601

Hunt, J. H., & Richard, F.-J. (2013). Intracolony vibroacoustic communication in social 602

insects. Insectes Sociaux, 60, 403-417. 603

Janssen, E., Bestmann, H. J., Hölldobler, B., & Kern, F. (1995). N,N-dimethyluracil and 604

actinidine, two pheromones of the ponerine and Megaponera foetens (Fab.) 605

(Hymenoptera: Formicidae). Journal of Chemical Ecology, 21, 1947 - 1955. 606

Kirchner W. H. (1997) Acoustical communication in social insects. In: M. Lehrer (ed)

607

Orientation and communication in arthropods (pp. 273 – 300). Basel: Birkhäuser

608

Lenoir, A., D'Ettorre, P., Errard, C., & Hefetz, A. (2001). Chemical ecology and social 609

parasitism in ants. Annual Review of Entomology, 46, 573-599. 610

Malicky, H. (1969). Versuch einer Analyse der ökologischen Beziehungen zwischen 611

Lycaeniden (Lepidoptera) und Formiciden (Hymenoptera). Tijdschrift voor 612

Entomologie, 112, 213 - 298. 613

Markl, H. (1965). Stridulation in Leaf-Cutting ants. Science, 149, 1392 - 1393. 614

Markl, H. (1967). Die Verständigung durch Stridulationssignale bei Blattschneiderameisen: I 615

Die biologische Bedeutung der Stridulation. Zeitschrift für vergleichende Physiologie, 616

57, 299 - 330. 617

(26)

Page 25 of 31 Markl, H. (1973, September). The evolution of stridulatory communication in ants.

618

In Proceedings of the International Congress IUSSI, London (Vol. 7, pp. 258-265). 619

Martin, S. J., & Drijfhout, F. P. (2009). A review of ant cuticular hydrocarbons. Journal of 620

Chemical Ecology, 35, 1151-1161. 621

Menzel, J. G., & Tautz, J. (1994). Functional morphology of the subgenual organ of the 622

carpenter ant. Tissue and Cell, 26, 735 - 746. 623

Nash, D. R., & Boomsma, J. J. (2008). Communication between hosts and social parasites. 624

In P. d'Ettore & D. P. Hughes (Eds.), Sociobiology of Communication (pp. 55 - 79). 625

Oxford: Oxford University Press. 626

Pech, P., Fric, Z., Konvicka, M., & Zrzavy, J. (2004). Phylogeny of Maculinea blues 627

(Lepidoptera : Lycaenidae) based on morphological and ecological characters: 628

evolution of parasitic myrmecophily. Cladistics-the International Journal of the Willi 629

Hennig Society, 20, 362-375. 630

Pellissier, L., Litsios, G., Guisan, A., & Alvarez, N. (2012). Molecular substitution rate 631

increases in myrmecophilous lycaenid butterflies (Lepidoptera). Zoologica Scripta, 632

41, 651-658 633

Pierce, N. E., Braby, M. F., Heath, A., Lohman, D. J., Mathew, J., Rand, D. B., & Travassos, 634

M. A. (2002). The ecology and evolution of ant association in the Lycaenidae 635

(Lepidoptera). Annual Review of Entomology, 47, 733-771. 636

Pierce, N. E., Kitching, R. L., Buckley, R. C., Taylor, M. F. J., & Benbow, K. F. (1987). The 637

Costs and Benefits of Cooperation between the Australian Lycaenid Butterfly, 638

Jalmenus evagoras, and Its Attendant Ants. Behavioral Ecology and Sociobiology, 639

21, 237-248. 640

R Core Team. (2015). R: A Language and Environment for Statistical Computing. Vienna, 641

Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-642

project.org 643

Riva, F., Barbero, F., Bonelli, S., Balletto, E., & Casacci, L. P. (in press). The acoustic 644

repertoire of lycaenid butterfly larvae. Bioacoustics. 645

(27)

Page 26 of 31 Roces, F., & Hölldobler, B. (1995). Vibrational communication between hitchhikers and 646

foragers in leaf-cutting ants (Atta cephalotes). Behavioral Ecology and Sociobiology, 647

37, 297-302. 648

Roces, F., & Hölldobler, B. (1996). Use of stridulation in foraging leaf cutting ants: 649

Mechanical support during cutting or short range recruitment signal? Behavioral 650

Ecology and Sociobiology, 39, 293-299. 651

Roces, F., & Tautz, J. (2001). Ants are deaf. Journal of the Acoustical Society of America, 652

109, 3080-3083. 653

Roces, F., Tautz, J., & Hölldobler, B. (1993). Stridulations in leaf-cutting ants. 654

Naturwissenschaften, 80, 521 - 524. 655

Ross, G. N. (1966). Life history studies on Mexican butterflies. IV. The ecology and ethology 656

of Anatole rossi, a myrmecophilous metalmark (Lepidoptera: Riodinidae). Annals of 657

the Entomological Society of America, 59, 985 - 1004. 658

Ruiz, E., Martinez, M. H., Martinez, M. D., & Hernandez, J. M. (2006). Morphological study of 659

the Stridulatory Organ in two species of Crematogaster genus: Crematogaster 660

scutellaris (Olivier 1792) and Crematogaster auberti (Emery 1869) (Hymenoptera : 661

Formicidae). Annales De La Societe Entomologique De France, 42, 99-105. 662

Sala, M., Casacci, L. P., Balletto, E., Bonelli, S., & Barbero, F. (2014). Variation in butterfly 663

larval acoustics as a strategy to infiltrate and exploit host ant colony resources. PLoS 664

One, 9, e94341. doi: 10.1371/journal.pone.0094341 665

Schurian, K. G., & Fiedler, K. (1991). Einfache Methoden zur Schallwahrnehmung bei 666

Bläulings-Larven (Lepidoptera: Lycaenidae). Entomologische Zeitschrift, 101, 393-667

412. 668

Tautz, J., Roces, F., & Hölldobler, B. (1995). Use of a sound based vibratome by leaf-cutting 669

ants. Science, 267, 84 - 87. 670

Thomas, J. A., Elmes, G. W., Schönrogge, K., Simcox, D. J., & Settele, J. (2005). Primary 671

hosts, secondary hosts and 'non-hosts': common confusions in the interpretation of 672

host specificity in Maculinea butterflies and other social parasites of ants. In J. 673

(28)

Page 27 of 31 Settele, E. Kühn & J. A. Thomas (Eds.), Studies on the ecology and conservation of 674

butterflies in Europe, vol. 2. (pp. 99 – 104). Sofia: Pensoft. 675

Thomas, J. A., Elmes, G. W., Sielezniew, M., Stankiewicz-Fiedurek, A., Simcox, D. J., 676

Settele, J., & Schonrogge, K. (2013). Mimetic host shifts in an endangered social 677

parasite of ants. Proceedings of the Royal Society B-Biological Sciences, 280, 678

20122336. http://dx.doi.org/10.1098/rspb.2012.2336 . 679

Thomas, J. A., Schönrogge, K., Bonelli, S., Barbero, F., & Balletto, E. (2010). Corruption of 680

ant acoustical signals by mimetic social parasites: Maculinea butterflies achieve 681

elevated status in host societies by mimicking the acoustics of queen ants. 682

Communicative & Integrative Biology, 3, 169-171. 683

Thomas, J. A., Schönrogge, K., & Elmes, G. W. (2005). Specializations and Host 684

Associations of Social Parasites of Ants. In M. D. E. Fellowes, G. J. Holloway & J. 685

Rolff (Eds.), Insect Evolutionary Ecology (pp. 475 - 514). London: Royal 686

Entomological Society. 687

Travassos, M. A., DeVries, P. J., & Pierce, N. E. (2008). A novel organ and mechanism for 688

larval sound production in butterfly caterpillars: Eurybia elvina. Tropical Lepidoptera 689

18, 20-23. 690

Travassos, M. A., & Pierce, N. E. (2000). Acoustics, context and function of vibrational 691

signalling in a lycaenid butterfly-ant mutualism. Animal Behaviour, 60, 13-26. 692

van Wilgenburg, E., Symonds, M. R., & Elgar, M. A. (2011). Evolution of cuticular 693

hydrocarbon diversity in ants. Journal of Evolutionary Biology, 24, 1188-1198. 694

vander Meer, R. K., & Morel, L. (1998). Nestmate Recognition in Ants. In R. K. vander Meer, 695

M. D. Breed, M. L. Winston & K. E. Espelie (Eds.), Pheromone Communication in 696

Social Insects (pp. 79 - 103). Oxford: Westview Press. 697

von Thienen, W., Metzler, D., Choe, D.-H., & Witte, V. (2014). Pheromone communication in 698

ants: a detailed analysis of concentration-dependent decisions in three species. 699

Behavioral Ecology and Sociobiology, 68, 1611-1627. 700

Wasmann, E. (1913). The ants and their guests. Smithonian Rep, 1912, 455 - 474. 701

(29)

Page 28 of 31 Wheeler, W. M. (1910). Ants:their structure, development and behavior (Vol. Vol. 9). New 702

York: Columbia University Press. 703

Wild, A. L. (2005). Taxonomic revision of the Pachycondyla apicalis species complex 704

(Hymenoptera: Formicidae). Zootaxa, 834, 1 - 25. 705

Winston, M. L. (1992). Semiochemicals and insect sociality. In B. D. Roitberg & M. B. Isman 706

(Eds.), Insect Chemical Ecology and Evolutionary Approach (pp. 315 - 333). London: 707

Chapman & Hall. 708

Witek, M., Barbero, F., & Marko, B. (2014). Myrmica ants host highly diverse parasitic 709

communities: from social parasites to microbes. Insectes Sociaux, 61, 307-323. 710

(30)

Page 29 of 31 Figures

711

Figure 1. The comparative morphology of sound production organs in myrmecophiles and 712

host ants. (a-e) the riodinids Synargis gela and Thisbe irenea (Riodinidae); larva (f, g) and 713

pupa (h-j) of the obligate lycaenid social parasite Maculinea rebeli and its adult host ant 714

Myrmica schencki (k-o); the adult beetle Paususs favieri (p-t) and its host Pheidole pallidula 715

(u-y). (a) Frontal view of Synargis gela head showing typical position of the riodinid vibratory 716

papillae; (b) general view of Thisbe irenea anterior edge of segment T-1 showing a vibratory 717

papilla (arrow) and the surface of the epicranium where the vibratory papilla strikes; (c) detail 718

of the vibratory papilla showing the annulations on its shaft and the epicranial granulations; 719

(d) enlarged view of the epicranial granulation and vibratory papilla; (e) details showing two 720

sizes of epicranial granulations. (f) Position of (g) the presumed sound producing organ of 721

Maculinea rebeli caterpillars and of its pupa (h), formed by a stridulatory plate (pars stridens) 722

placed on the fifth abdominal segment and a file (plectrum) in the sixth abdominal segment. 723

(k,p,u) Respective positions of the stridulatory organs of Myrmica schencki, Paussus favieri 724

and Pheidole pallidula; the organs are composed of suboval pars stridens (l,q,v) with minute 725

ridges (m,r,w) and a plectrum (n, x) consisting of a medial cuticular prominence (t,y) that 726

originates from the posterior edge of the postpetiole in the two ant species or of a curved row 727

of small cuticular spines in P. favieri (s,t). (a, modified by De Vries 1991; b-e modified by 728

DeVries 1988; p-y modified by Di Giulio et al. 2015). 729

730

Figure 2. A diagram of the phylogeny (left) and the cluster analysis constructed from a matrix 731

of pairwise normalized Euclidean distances of the sound profiles from three caterpillars of 13 732

species of lycaenid. Symbols and values refer to the intensity of interaction of the lycaenid 733

species with their host ants (0 = none; 4 = social parasite), following Fiedler (1991). 734

735 736 737 738

(31)

Page 30 of 31 Figure 1: 739 740 741 742 743 744 745 746 747 748 749

(32)

Page 31 of 31 Figure 2:

750

Riferimenti

Documenti correlati

Studies at The University of Turin are using flow cytometry to investigate if tumour cell DNA content (ploidy and cell cycle), proliferative activity and apoptosis are

La domanda che ha suscitato un vivace dibattito tra studiosi seguaci delle teorie critiche di stampo francofortese e quelli più inclini a visioni posi- tiviste dei fenomeni sociali

In this manuscript, we devise a leader-follower coop- erative control strategy for formation control in groups of planar non-holonomic unicycle mobile robots, that is capable of

Indeed, personalized nutrition recommendations based also on the individual ’s genetic background might improve the outcomes of a speci fic dietary intervention and could represent a

Fra l’avventura notturna in cui Pyle salva la vita a Fowler e il compimento di un percorso umano che spinge Fowler ad assumersi la responsabilità della morte di

Inside these tubular structures, formed by the ingrowth of the root hair cell walls from the point of penetration of rhizobia, bacterial invasion proceed to the root cortical

For a generic affine space L of codimension s and a generic matrix U in L, the polynomial system 2.4 has finitely many complex solutions which correspond to the critical points of

Axial compressors (ACs) are usually preferred in high power gas turbine applications, indeed they can achieve higher mass flow rate, even if the high pressure rise is achieved using